{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,8]],"date-time":"2026-07-08T01:12:27Z","timestamp":1783473147657,"version":"3.55.0"},"reference-count":37,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2021,9,13]],"date-time":"2021-09-13T00:00:00Z","timestamp":1631491200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000066","name":"National Institute of Environmental Health Sciences","doi-asserted-by":"publisher","award":["R01ES016772"],"award-info":[{"award-number":["R01ES016772"]}],"id":[{"id":"10.13039\/100000066","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000066","name":"National Institute of Environmental Health Sciences","doi-asserted-by":"publisher","award":["P30ES025128"],"award-info":[{"award-number":["P30ES025128"]}],"id":[{"id":"10.13039\/100000066","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000066","name":"National Institute of Environmental Health Sciences","doi-asserted-by":"publisher","award":["P01ES022831"],"award-info":[{"award-number":["P01ES022831"]}],"id":[{"id":"10.13039\/100000066","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000066","name":"National Institute of Environmental Health Sciences","doi-asserted-by":"publisher","award":["R24ES028531"],"award-info":[{"award-number":["R24ES028531"]}],"id":[{"id":"10.13039\/100000066","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000139","name":"U.S. Environmental Protection Agency","doi-asserted-by":"publisher","award":["RD-83543701"],"award-info":[{"award-number":["RD-83543701"]}],"id":[{"id":"10.13039\/100000139","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100009633","name":"Eunice Kennedy Shriver National Institute of Child Health and Human Development","doi-asserted-by":"publisher","award":["R01HD084487"],"award-info":[{"award-number":["R01HD084487"]}],"id":[{"id":"10.13039\/100009633","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Nutrients"],"abstract":"<jats:p>Maternal periconceptional diets have known associations with proper offspring neurodevelopment. Mechanisms for such associations include improper energy\/nutrient balances between mother and fetus, as well as altered offspring epigenetics during development due to maternal nutrient and inflammatory status. Using a comprehensive food frequency questionnaire and assessing offspring temperament with the Infant-Toddler Social and Emotional Assessment (n = 325, mean age = 13.9 months), we sought to test whether a maternal periconceptional diet characterized by high glycemic loading (MGL) would affect offspring temperament using adjusted ordinal regression. After limiting false discovery to 10%, offspring born to mothers in tertile 3 of glycemic loading (referent = tertile 1) were more likely to be in the next tertile of anxiety [OR (95% CI) = 4.51 (1.88\u201311.07)] and inhibition-related behaviors [OR (95% CI) = 3.42 (1.49\u20137.96)]. Male offspring were more likely to exhibit impulsive [OR (95% CI) = 5.55 (1.76\u201318.33)], anxiety [OR (95% CI) = 4.41 (1.33\u201315.30)], sleep dysregulation [OR (95% CI) = 4.14 (1.34\u201313.16)], empathy [6.68 (1.95\u201324.40)], and maladaptive behaviors [OR (95% CI) = 9.86 (2.81\u201337.18)], while females were more likely to exhibit increased anxiety-related behaviors [OR (95% CI) = 15.02 (3.14\u201384.27)]. These associations persisted when concurrently modeled with the maternal\u2013Mediterranean dietary pattern. In a subset (n = 142), we also found MGL associated with increased mean methylation of the imprint control region of SGCE\/PEG10. In conclusion, these findings highlight the importance of maternal dietary patterns on offspring neurodevelopment, offering avenues for prevention options for mothers.<\/jats:p>","DOI":"10.3390\/nu13093180","type":"journal-article","created":{"date-parts":[[2021,9,13]],"date-time":"2021-09-13T23:32:23Z","timestamp":1631575943000},"page":"3180","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":10,"title":["Periconceptional Maternal Diet Characterized by High Glycemic Loading Is Associated with Offspring Behavior in NEST"],"prefix":"10.3390","volume":"13","author":[{"given":"Candice L.","family":"Alick","sequence":"first","affiliation":[{"name":"Center for Health Promotion and Disease Prevention, University of North Carolina at Chapel Hill, Chapel Hill, NC 27514, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rachel L.","family":"Maguire","sequence":"additional","affiliation":[{"name":"Center for Human Health and the Environment, North Carolina State University, Raleigh, NC 27695, USA"},{"name":"Department of Biological Sciences, North Carolina State University, Raleigh, NC 27695, USA"},{"name":"Department of Obstetrics and Gynecology, Duke University Medical Center, Durham, NC 27701, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8298-7272","authenticated-orcid":false,"given":"Susan K.","family":"Murphy","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology, Duke University Medical Center, Durham, NC 27701, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bernard F.","family":"Fuemmeler","sequence":"additional","affiliation":[{"name":"Department of Health Behavior and Policy, Virginia Commonwealth University, Richmond, VA 23219, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Cathrine","family":"Hoyo","sequence":"additional","affiliation":[{"name":"Center for Human Health and the Environment, North Carolina State University, Raleigh, NC 27695, USA"},{"name":"Department of Biological Sciences, North Carolina State University, Raleigh, NC 27695, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8447-7871","authenticated-orcid":false,"given":"John S.","family":"House","sequence":"additional","affiliation":[{"name":"Center for Human Health and the Environment, North Carolina State University, Raleigh, NC 27695, USA"},{"name":"Biostatistics and Computational Biology Branch, National Institute of Environmental Health Sciences, National Institutes of Health, Department of Health and Human Services, Research Triangle Park, Durham, NC 27709, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,9,13]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1016\/j.jpeds.2017.04.065","article-title":"Maternal Nutrition and Child Neurodevelopment: Actions Across Generations","volume":"187","author":"Miller","year":"2017","journal-title":"J. Pediatr."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"612705","DOI":"10.3389\/fncel.2020.612705","article-title":"From Maternal Diet to Neurodevelopmental Disorders: A Story of Neuroinflammation","volume":"14","author":"Bordeleau","year":"2020","journal-title":"Front. Cell Neurosci."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"107","DOI":"10.3389\/fcell.2018.00107","article-title":"Periconceptional Maternal Mediterranean Diet Is Associated With Favorable Offspring Behaviors and Altered CpG Methylation of Imprinted Genes","volume":"6","author":"House","year":"2018","journal-title":"Front. Cell Dev. Biol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1828","DOI":"10.1016\/j.jada.2004.09.029","article-title":"More favorable dietary patterns are associated with lower glycemic load in older adults","volume":"104","author":"Davis","year":"2004","journal-title":"J. Am. Diet. Assoc."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"e016777","DOI":"10.1136\/bmjopen-2017-016777","article-title":"The importance of maternal diet quality during pregnancy on cognitive and behavioural outcomes in children: A systematic review and meta-analysis","volume":"7","author":"Borge","year":"2017","journal-title":"BMJ Open"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"676","DOI":"10.3945\/ajcn.114.084905","article-title":"Maternal dietary glycemic index and glycemic load in early pregnancy are associated with offspring adiposity in childhood: The Southampton Women\u2019s Survey","volume":"100","author":"Okubo","year":"2014","journal-title":"Am. J. Clin. Nutr."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1471","DOI":"10.1017\/S0007114512003443","article-title":"Maternal dietary glycaemic load during pregnancy and gestational weight gain, birth weight and postpartum weight retention: A study within the Danish National Birth Cohort","volume":"109","author":"Knudsen","year":"2013","journal-title":"Br. J. Nutr."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1016\/j.clnu.2013.03.002","article-title":"Maternal dietary patterns during pregnancy and child internalising and externalising problems. The Generation R Study","volume":"33","author":"Tiemeier","year":"2014","journal-title":"Clin. Nutr."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"88","DOI":"10.1017\/S2040174415000124","article-title":"Maternal diet as a modifier of offspring epigenetics","volume":"6","author":"Lillycrop","year":"2015","journal-title":"J. Dev. Orig. Health Dis."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"4046","DOI":"10.1093\/hmg\/ddp353","article-title":"DNA methylation differences after exposure to prenatal famine are common and timing- and sex-specific","volume":"18","author":"Tobi","year":"2009","journal-title":"Hum. Mol. Genet."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1111\/jcpp.12589","article-title":"Prenatal unhealthy diet, insulin-like growth factor 2 gene (IGF2) methylation, and attention deficit hyperactivity disorder symptoms in youth with early-onset conduct problems","volume":"58","author":"Rijlaarsdam","year":"2017","journal-title":"J. Child. Psychol. Psychiatry"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"495","DOI":"10.1023\/A:1025449031360","article-title":"The Infant-Toddler Social and Emotional Assessment (ITSEA): Factor structure, reliability, and validity","volume":"31","author":"Carter","year":"2003","journal-title":"J. Abnorm. Child. Psychol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1007\/s10802-009-9342-0","article-title":"Internalizing trajectories in young boys and girls: The whole is not a simple sum of its parts","volume":"38","author":"Carter","year":"2010","journal-title":"J. Abnorm. Child Psychol."},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Kruizinga, I., Visser, J.C., van Batenburg-Eddes, T., Carter, A.S., Jansen, W., and Raat, H. (2014). Screening for autism spectrum disorders with the brief infant-toddler social and emotional assessment. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0097630"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"560","DOI":"10.1093\/ajcn\/73.3.560","article-title":"Dietary glycemic load assessed by food-frequency questionnaire in relation to plasma high-density-lipoprotein cholesterol and fasting plasma triacylglycerols in postmenopausal women","volume":"73","author":"Liu","year":"2001","journal-title":"Am. J. Clin. Nutr."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1455","DOI":"10.1093\/ajcn\/71.6.1455","article-title":"A prospective study of dietary glycemic load, carbohydrate intake, and risk of coronary heart disease in US women","volume":"71","author":"Liu","year":"2000","journal-title":"Am. J. Clin. Nutr."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"992","DOI":"10.3945\/ajcn.111.012138","article-title":"Calculating meal glycemic index by using measured and published food values compared with directly measured meal glycemic index","volume":"94","author":"Dodd","year":"2011","journal-title":"Am. J. Clin. Nutr."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"59","DOI":"10.4137\/GEG.S40538","article-title":"DNA Methylation of Regulatory Regions of Imprinted Genes at Birth and Its Relation to Infant Temperament","volume":"8","author":"Fuemmeler","year":"2016","journal-title":"Genet. Epigenet."},{"key":"ref_19","first-page":"dvx007","article-title":"Low maternal adherence to a Mediterranean diet is associated with increase in methylation at the MEG3-IG differentially methylated region in female infants","volume":"3","author":"Mendez","year":"2017","journal-title":"Environ. Epigenet."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Murphy, S.K., Huang, Z., and Hoyo, C. (2012). Differentially methylated regions of imprinted genes in prenatal, perinatal and postnatal human tissues. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0040924"},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Nye, M.D., Hoyo, C., Huang, Z., Vidal, A.C., Wang, F., Overcash, F., Smith, J.S., Vasquez, B., Hernandez, B., and Swai, B. (2013). Associations between methylation of paternally expressed gene 3 (PEG3), cervical intraepithelial neoplasia and invasive cervical cancer. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0056325"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1111\/j.2517-6161.1995.tb02031.x","article-title":"Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing","volume":"57","author":"Benjamini","year":"1995","journal-title":"J. R. Stat. Soc. Ser. B (Methodological)"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1933","DOI":"10.3892\/ijo.2016.3406","article-title":"PEG10 promotes human breast cancer cell proliferation, migration and invasion","volume":"48","author":"Li","year":"2016","journal-title":"Int. J. Oncol."},{"key":"ref_24","first-page":"3043","article-title":"Involvement of PEG10 in human hepatocellular carcinogenesis through interaction with SIAH1","volume":"63","author":"Okabe","year":"2003","journal-title":"Cancer Res."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1007\/s10238-015-0350-9","article-title":"Upregulation of long noncoding RNA PEG10 associates with poor prognosis in diffuse large B cell lymphoma with facilitating tumorigenicity","volume":"16","author":"Peng","year":"2016","journal-title":"Clin. Exp. Med."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"182","DOI":"10.1038\/modpathol.2015.144","article-title":"High-definition CpG methylation of novel genes in gastric carcinogenesis identified by next-generation sequencing","volume":"29","author":"Sepulveda","year":"2016","journal-title":"Mod. Pathol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"90","DOI":"10.1186\/s13148-018-0521-0","article-title":"DNA methylation of imprinted genes at birth is associated with child weight status at birth, 1 year, and 3 years","volume":"10","author":"Mendez","year":"2018","journal-title":"Clin. Epigenet."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"351","DOI":"10.4161\/epi.27160","article-title":"Differentially methylated regions in maternal and paternal uniparental disomy for chromosome 7","volume":"9","author":"Muurinen","year":"2014","journal-title":"Epigenetics"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"985","DOI":"10.1016\/j.jnutbio.2014.04.012","article-title":"Hippocampal apoptosis involved in learning deficits in the offspring exposed to maternal high sucrose diets","volume":"25","author":"Kuang","year":"2014","journal-title":"J. Nutr. Biochem."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Ruskin, D.N., Murphy, M.I., Slade, S.L., and Masino, S.A. (2017). Ketogenic diet improves behaviors in a maternal immune activation model of autism spectrum disorder. PLoS ONE, 12.","DOI":"10.1371\/journal.pone.0171643"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"354","DOI":"10.1159\/000439087","article-title":"Prenatal Exposure to Maternal Obesity Alters Anxiety and Stress Coping Behaviors in Aged Mice","volume":"103","author":"Balsevich","year":"2016","journal-title":"Neuroendocrinology"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"898","DOI":"10.1016\/j.biopsych.2019.12.004","article-title":"Persistently High Levels of Maternal Antenatal Inflammation Are Associated With and Mediate the Effect of Prenatal Environmental Adversities on Neurodevelopmental Delay in the Offspring","volume":"87","author":"Girchenko","year":"2020","journal-title":"Biol. Psychiatry"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"550","DOI":"10.1016\/j.biopsych.2020.10.008","article-title":"Dietary Quality and Dietary Inflammatory Potential During Pregnancy and Offspring Emotional and Behavioral Symptoms in Childhood: An Individual Participant Data Meta-analysis of Four European Cohorts","volume":"89","author":"Polanska","year":"2021","journal-title":"Biol. Psychiatry"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"518","DOI":"10.1093\/humupd\/dmz017","article-title":"Transgenerational inheritance: How impacts to the epigenetic and genetic information of parents affect offspring health","volume":"25","author":"Xavier","year":"2019","journal-title":"Hum. Reprod. Update"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"e1103","DOI":"10.1038\/tp.2017.74","article-title":"Influences of prenatal and postnatal maternal depression on amygdala volume and microstructure in young children","volume":"7","author":"Wen","year":"2017","journal-title":"Transl. Psychiatry"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1016\/j.euroneuro.2010.07.004","article-title":"Evidence of female-specific glial deficits in the hippocampus in a mouse model of prenatal stress","volume":"21","author":"Behan","year":"2011","journal-title":"Eur. Neuropsychopharmacol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"320","DOI":"10.1111\/j.1365-2826.2011.02117.x","article-title":"Differential effect of prenatal stress on the expression of corticotrophin-releasing hormone and its receptors in the hypothalamus and amygdala in male and female rats","volume":"23","author":"Zohar","year":"2011","journal-title":"J. Neuroendocrinol."}],"container-title":["Nutrients"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2072-6643\/13\/9\/3180\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T07:01:32Z","timestamp":1760166092000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2072-6643\/13\/9\/3180"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,9,13]]},"references-count":37,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2021,9]]}},"alternative-id":["nu13093180"],"URL":"https:\/\/doi.org\/10.3390\/nu13093180","relation":{},"ISSN":["2072-6643"],"issn-type":[{"value":"2072-6643","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,9,13]]}}}